my thoughts on science

A new pied babbler paper has come out from Martha Nelson-Flower. Martha looked at how long subordinates stayed in their groups and how likely they were to gain a dominant breeding position. In babblers there appears to be a sex difference: males have a longer subordinate tenure when they are related to the dominant male, but there is no impact of relatedness for females (either relatedness to the dominant female or male). But why is this important? Well, it turns out that the longer you are a subordinate for then the more likely you are to attain dominance.

Why would this be the case? Well it may be that dominant males are less tolerant of unrelated males, as they are more likely to compete with them for reproductive opportunities. Related males in pied babbler groups tend to be father and son (with dad being dominant), although it can be the case that one brothers holds the dominant position while the other is subordinate. But why would sticking around as a subordinate be better? Surely it pays to leave quickly and get a dominant position elsewhere, so you yourself can breed. However, gaining dominance is not that easy, vacancies are not that easy to come by and you have to be a pretty big and sexy male to just go and kick another male out of his group. Perhaps it is best just to stay in a group, build up your condition and wait for an opportunity, as going it alone is a very risky business for a babbler!

Nepotism and subordinate tenure in a cooperative breeder. Biology LettersIn many cooperatively breeding societies, subordinate individuals delay dispersal and independent breeding. The length of time that subordinates delay dispersal (subordinate tenure) is likely to have important implications for both subordinate and dominant fitness. However, quantitative comparisons of the subordinate tenure of males and females are rare, especially with respect to the presence of same- versus opposite-sex close kin. Here, we investigate subordinate tenure and how it is affected by the genetic relationship between subordinates and dominants in the cooperatively breeding southern pied babbler (Turdoides bicolor). We find that for males, longer subordinate tenures result in increased likelihood of attaining dominance. In the presence of an unrelated dominant male, tenure of subordinate males is significantly shorter, indicating nepotism among males. Female tenures are unaffected by the genetic relationship to either the dominant male or female. These results are some of the first to demonstrate that the sex of both the dominants and subordinates, and the genetic relationship between them, can have significant impacts on subordinate tenure and dispersal delays. Nepotism has likely played a vital role in the evolution of cooperative breeding in this species.

Some new papers have come out from both the Pied Babbler Project and the Arabian Babbler Project. I’ve put the abstracts and links below. This is a very quick blog, basically trying to get people to read these two great papers.

The first is Sabrina Engesser’s work into vocal communication and syntax in pied babblers. Using observations and playback experiments, Sabrina has been able to show that the order in which alarm and mobbing calls are given is highly important for these group living birds. Syntax is something that humans use and has been observed in primates but never in birds. This ground breaking work is important for understand how language may have evolved and how widespread some of the components of our communication are in the natural world.

The second is from Oded Keynan, this time looking at population dynamics instead of his normal social learning research. This new work shows that the group living Arabian babblers suffer the population and group effects of the Allee effect. Larger groups are better able to rear young and persist than smaller groups, and this isn’t just on a group level but also denser populations do better as well. Interestingly, however, immigration and emigration don’t really have an effect.

I hope you have a read, because they’re two great bits of research.

Meaningful call combinations and compositional processing in the southern pied babbler. PNASLanguage’s expressive power is largely attributable to its compositionality: meaningful words are combined into larger/higher-order structures with derived meaning. Despite its importance, little is known regarding the evolutionary origins and emergence of this syntactic ability. Although previous research has shown a rudimentary capability to combine meaningful calls in primates, because of a scarcity of comparative data, it is unclear to what extent analog forms might also exist outside of primates. Here, we address this ambiguity and provide evidence for rudimentary compositionality in the discrete vocal system of a social passerine, the pied babbler (Turdoides bicolor). Natural observations and predator presentations revealed that babblers produce acoustically distinct alert calls in response to close, low-urgency threats and recruitment calls when recruiting group members during locomotion. On encountering terrestrial predators, both vocalizations are combined into a “mobbing sequence,” potentially to recruit group members in a dangerous situation. To investigate whether babblers process the sequence in a compositional way, we conducted systematic experiments, playing back the individual calls in isolation as well as naturally occurring and artificial sequences. Babblers reacted most strongly to mobbing sequence playbacks, showing a greater attentiveness and a quicker approach to the loudspeaker, compared with individual calls or control sequences. We conclude that the sequence constitutes a compositional structure, communicating information on both the context and the requested action. Our work supports previous research suggesting combinatoriality as a viable mechanism to increase communicative output and indicates that the ability to combine and process meaningful vocal structures, a basic syntax, may be more widespread than previously thought.

Component, group and demographic Allee effects in a cooperatively breeding bird species, the Arabian babbler (Turdoides squamiceps). OecologiaIn population dynamics, inverse density dependence can be manifested by individual fitness traits (component Allee effects), and population-level traits (demographic Allee effects). Cooperatively breeding species are an excellent model for investigating the relative importance of Allee effects, because there is a disproportionately larger benefit to an individual of being part of a large group. As a consequence, larger groups have greater performance than small groups, known as the group Allee effect. Although small populations of cooperative breeders may be prone to all levels of Allee effects, empirical evidence for the existence of a demographic Allee effects is scarce. To determine the extent to which Allee effects are present in a cooperatively breeding species, we used a comprehensive 35-year life history database for cooperatively breeding Arabian babblers (Turdoides squamiceps). Firstly, we confirmed the existence of a component Allee effect by showing that breeding individuals in large groups receive greater benefits than those in small groups; second, we confirmed the existence of group Allee effect by showing that larger groups survive longer. And thirdly, we identified a demographic Allee effect by showing that per capita population growth rate is positively affected by population density. Finally, we found that emigration and immigration rates, although dependent on group size, do not buffer against component and group-level Allee effects becoming a demographic Allee effect. Our finding of the existence of all three levels of Allee effects in a cooperative breeder may have important implications for future research and conservation decisions.

This morning I awoke to a science media awash with reporting on a new paper produced from a field site that I spent many years at. The work is a new paper, published in Nature, on meerkats and competitive growth. To name (and link) just a few of the news stories, it was covered by the Guardian, Science, Science Daily and National Geographic – pretty widespread and prestigious, not to mention far reaching, media coverage. I don’t want to go into all the ins and outs of this new bit of research, as exciting as it is, as you can just click on the above links or read the article yourself (link and abstract at the end). But the gist is that in meerkat litters, if your siblings are growing faster than you then you increase your food intake and growth rate to try and match them, this was elucidated using some really great experiments (details of that later). This is really important for cooperatively breeding species like meerkats, where reproductive skew is high with only a few individuals ever reaching dominance. So in order to maximise their chances of competing with their litter mates, meerkat pups up their food intake. Simples!

What I want to briefly expand on here is the importance of long-term research in this discovery. The study animals used for this work are wild, they all live out their lives in the Kalahari and are beset by the hardships of competition, constant foraging and threats of predation. However, these meerkats (like the babblers that I worked on) are habituated to human observation. This habituation has huge benefits, it allows close observation of interactions, it allows for identifying individuals, it allows for field experiments to be done (be they playing back specific calls or tactically feeding specific meerkats as they did here!) but in the case of the meerkats (and the babblers) it allows researchers to weigh them multiple times a day. You may ask what does this have to do with long-term research? Well meerkats are naturally very skittish, they’re not very big and lots of things want to eat them. It typically takes between 12-24 months to habituate a group up to a good level, from spending hours sitting at a burrow as still as possible but humming the habituation song all the way to walking with them and weighing them. And to have a study population of between 16-25 groups that is a lot of man hours. To get around all of those groups on a regular enough basis you need a small army of researchers, constantly collecting weights, life-history data and helping out with experiments.

The benefits of long-term studies including being able to weigh the animals. For example this pied babbler.

This work is also built upon decades worth of other research on these animals, which is not possible without uninterrupted observation. Slowly but surely this work unravelled the natural history of these animals, opening up interesting research questions, which in turn attract researchers with other interest that open up new avenues of research. Long-term studies thus offer a great avenue to expand our knowledge just simply by persisting in one place over a long time. They also tend to build up a network/family tree of researchers who have either worked or done PhDs or post-docs there, and once they move on they are a valuable link between research institutions. Ironically, even though the meerkats have been shown to not be very incestuous, the meerkat research are less averse to such behaviour!

All of these ideas are summed up in a great paper entitled: Individuals and populations: the role of long-term, individual-based studies of animals in ecology and evolutionary biology. Long-term study populations exist in many species across all taxa. The meerkats, red deer, Arabian babblers, blue tits, marmots, big horn sheep and pied babblers are just the ones that come off the top of my head. All of these have contributed massively to our understanding of behavioural ecology, population biology and conservation. So when I see a paper like this new meerkat paper I don’t just see the work of the named authors (shout out to Matt Bell – legend) but also to the tens to hundreds of volunteer researchers who have kept those projects going over the decades of their existence (of which I was once one). I hope that after reading this that you’ll appreciate that too.

In many animal societies where hierarchies govern access to reproduction, the social rank of individuals is related to their age and weight1, 2, 3, 4, 5 and slow-growing animals may lose their place in breeding queues to younger ‘challengers’ that grow faster5, 6. The threat of being displaced might be expected to favour the evolution of competitive growth strategies, where individuals increase their own rate of growth in response to increases in the growth of potential rivals. Although growth rates have been shown to vary in relation to changes in the social environment in several vertebrates including fish2, 3, 7 and mammals8, it is not yet known whether individuals increase their growth rates in response to increases in the growth of particular reproductive rivals. Here we show that, in wild Kalahari meerkats (Suricata suricatta), subordinates of both sexes respond to experimentally induced increases in the growth of same-sex rivals by raising their own growth rate and food intake. In addition, when individuals acquire dominant status, they show a secondary period of accelerated growth whose magnitude increases if the difference between their own weight and that of the heaviest subordinate of the same sex in their group is small. Our results show that individuals adjust their growth to the size of their closest competitor and raise the possibility that similar plastic responses to the risk of competition may occur in other social mammals, including domestic animals and primates.

In the spirit of many of my previous blogs I am going to write about a new paper written by someone I know. This may sound like some sort of nepotism, not that many people really read my blog, but this new paper has actually made quite a splash and so I’m really just following a great new science story. If you want to see some of the other coverage then click on these links: Science, Sci News, Science Daily, or PLoS Blogs. (The abstract and link to the paper in question is at the bottom of the blog)

This new piece of research is a product of the Hot Birds team at the Fitz in Cape Town, with Tanja van de Ven (lead author) spending many gruelling hours in the Kalahari heat with fairly complex equipment. The team, and Tanja’s, aim is to investigate how birds cope with rising temperatures using species that already exist in the hard thermal conditions of the Kalahari. One of their papers looked at the impact of heat stress on foraging in pied babblers. However, Tanja’s work focuses on yellow-billed hornbills, a species of bird that nests inside trees, with the female sealing herself into this cavity. This reproductive adaptation is great for protecting your eggs and female from predators but it can limit your ability to control your temperature, as you’re pretty stuck (it also means that the female and chicks are 100% dependent on the male for their nutritional needs – such a cool system for male-female and parent-offspring dynamics!!!).

The obvious feature of this bird, hopefully you have either clicked on the link or already know what a hornbill looks like from your bird knowledge or from childhood exposure to the Lion King, is that they have a massive long bill. The beak of a bird is not just lifeless tissue like finger nails but very much a living structure and as such has a profusion of blood vessels. Just like the thermoregulation that takes place in humans, where capillaries close to the surface are constricted or relaxed to either conserve or radiate heat, hornbills appear to have the same ability with the blood vessels in their beak. As the ambient air temperature increases more blood is pushed into the hornbill’s beak, allowing heat to be lost through radiative heat transfer. This is similar to toucans, as a recent study has found, but in the toucan this process accounts for upto 60% of non-evaporative heat loss compared to just 8% in the hornbill. There are a number of potential reasons for this: the toucans have much larger bills, hornbills have a harder bill (maybe an ecological adaptation to how they forage?) and toucans start dilating their blood vessels at lower temperatures.

This type of research is crucial for understanding how organisms are physiologically adapted to their environment. It enables researchers to better understand the environmental limits that a species may be able to cope with and allow predictions as to the impacts of climate change. It’s also pretty cool too.

Beaks are increasingly recognised as important contributors to avian thermoregulation. Several studies supporting Allen’s rule demonstrate how beak size is under strong selection related to latitude and/or air temperature (Ta). Moreover, active regulation of heat transfer from the beak has recently been demonstrated in a toucan (Ramphastos toco, Ramphastidae), with the large beak acting as an important contributor to heat dissipation. We hypothesised that hornbills (Bucerotidae) likewise use their large beaks for non-evaporative heat dissipation, and used thermal imaging to quantify heat exchange over a range of air temperatures in eighteen desert-living Southern Yellow-billed Hornbills (Tockus leucomelas). We found that hornbills dissipate heat via the beak at air temperatures between 30.7°C and 41.4°C. The difference between beak surface and environmental temperatures abruptly increased when air temperature was within ~10°C below body temperature, indicating active regulation of heat loss. Maximum observed heat loss via the beak was 19.9% of total non-evaporative heat loss across the body surface. Heat loss per unit surface area via the beak more than doubled at Ta > 30.7°C compared to Ta < 30.7°C and at its peak dissipated 25.1 W m-2. Maximum heat flux rate across the beak of toucans under comparable convective conditions was calculated to be as high as 61.4 W m-2. The threshold air temperature at which toucans vasodilated their beak was lower than that of the hornbills, and thus had a larger potential for heat loss at lower air temperatures. Respiratory cooling (panting) thresholds were also lower in toucans compared to hornbills. Both beak vasodilation and panting threshold temperatures are potentially explained by differences in acclimation to environmental conditions and in the efficiency of evaporative cooling under differing environmental conditions. We speculate that non-evaporative heat dissipation may be a particularly important mechanism for animals inhabiting humid regions, such as toucans, and less critical for animals residing in more arid conditions, such as Southern Yellow-billed Hornbills. Alternatively, differences in beak morphology and hardness enforced by different diets may affect the capacity of birds to use the beak for non-evaporative heat loss.

There are many species that do not just exist with one specific colour pattern. These different colourations are called polymorphisms, existing in a variety of taxa from crabs to lizards to birds. There have been many explanations for the existence of these differences within a species, from protecting against predators to being important for mate choice. There is even a species of lizard, the side-blotched lizard, that exists in three colour morphs that are linked to their behaviour that was famously studied by Barry Sinervo. The orange males are more dominant, the blue males cooperate and the yellow males mimic females. These three morphs live in a state of perpetual flux as none can get the upper hand in the mating game. Basically colour morphs are interesting and we’ve really not touched the surface in understanding the evolutionary mechanisms that lead to and maintain them.

Some really cool studies have been done at the Percy FitzPatrick Institute in Cape Town by Arjun Amar to investigate the two colour morphs of the black sparrowhawk (Accipiter melanoleucus). These majestic birds are either a white or black morph. A new paper has just come out showing that one of the factors that may be keeping these morphs going is the difference in hunting success that they face. Black morphs, unsurprisingly because of their colour, have a higher success in low light levels, while their white breather have the opposite success rates. These success rates tie in with the breeding season of these morphs and may go a long way to explaining the variation in morph distribution across the species South African range. Abstract below:

Tate et al. (2016) Differential foraging success across a light level spectrum explains the maintenance and spatial structure of colour morphs in a polymorphic bird. Ecology LettersDetectability of different colour morphs under varying light conditions has been proposed as an important driver in the maintenance of colour polymorphism via disruptive selection. To date, no studies have tested whether different morphs have selective advantages under differing light conditions. We tested this hypothesis in the black sparrowhawk, a polymorphic raptor exhibiting a discrete white and dark morph, and found that prey provisioning rates differ between the morphs depending on light condition. Dark morphs delivered more prey in lower light conditions, while white morphs provided more prey in brighter conditions. We found support for the role of breeding season light level in explaining the clinal pattern of variation in morph ratio across the species range throughout South Africa. Our results provide the first empirical evidence supporting the hypothesis that polymorphism in a species, and the spatial structuring of morphs across its distribution, may be driven by differential selective advantage via improved crypsis, under varying light conditions.

These results tie in nicely with previous work that has looked at the ratio of morphs across South Africa. This work found that the Cape peninsula had a very high proportion of black morphs but that this was unlikely to do with a founder effect. More likely it was because of higher rainfall rates during the breeding season, fitting nicely with the recent hunting findings. However, as is often the case in biological systems, hunting and light are not the only potential drivers for polymorphism in this species. It turns out that black morphs have a lower parasite load than white morphs.

The great thing about this particular subsection of research on the black sparrowhawk is that it all initially came from the observation that there seemed to be more black morphs in Cape Town than normal. This simple natural history note has spawned a growing number of scientific papers and led to wonderful new insights into evolution. So the next time you notice something when walking about just think that it might be far more interesting than may initially be apparent!

A new paper on how Arabian babblers learn has just come out in Ethology. I've pasted the abstract and link below. This new work shows that dominant individuals are the fastest to learn to shift a learnt skill into a new context, from lifting black rubber lids to lifting white rubber lids, and that learned skills are transmitted horizontally between groups. The study of animal learning and how information is transferred between individuals is a fascinating field of behavioural science. In group living species the ability to learn new information, be it foraging skills or the dominance structure in your group, may be crucial for survival and an individuals prospects of achieving a reproductive position. I know that Oded spent many hours in the field collecting this data and this is a great paper!

Keynan et al. (2016) Task-dependent differences in learning by subordinate and dominant wild Arabian babblers. Ethology, DOI: 10.1111/eth.12488Learning and innovation abilities have been studied extensively in flocking birds, but their importance and relevance in cooperatively breeding birds have been relatively unexplored. We studied the acquisition of novel foraging skills in 14 groups of wild, cooperatively breeding Arabian babblers (Turdoides squamiceps). While in a previous study we found that subordinate individuals were usually the first to learn to remove black rubber lids from a foraging grid, here we show that dominant individuals were the first to succeed in shifting from these black rubber lids to newly introduced white rubber lids. We also found that in all groups where one forager learned to shift to the white lids, the rest of the foragers also learned to do so, suggesting that this behaviour may be transmitted among group members. Although dominant individuals were almost always the first to remove white lids, once starting to remove white lids, dominants and subordinates learned equally well to prefer white over black lids based on differential reinforcement (food was provided only under white lids). Together with our previous study, our results suggest that differences in learning between dominants and subordinates may be task-specific, which may represent different cognitive strategies: subordinates may explore a more diverse range of foraging opportunities, while dominants may be better at generalizing from familiar tasks to similar ones.

A great new piece of research has just been published by some of my old colleagues at the Fitz in Cape Town (Susie Cunningham and Arjun Amar). It’s work that I help with at its inception, and it shows that pied crows have changed their distribution in South Africa and it’s mainly due to changes in climate and the distribution in power lines. A great piece of research that shows how the twin human impacts of climate change and habitat modification are shaping the natural world.

AbstractAimClimate change and other anthropogenic global change drivers act in complex, mutually exacerbating ways to alter the abundance and distribution of species. In South Africa, pied crows Corvus albus have increased in numbers and range in recent decades. Popular opinion links these changes to urbanisation and infrastructure development, but there has been no empirical test of this idea. We aimed to clarify the drivers of pied crow population changes in South Africa.LocationSouth Africa.MethodsWe used publicly available long-term datasets, the Southern African Bird Atlas Project and University of Delaware Gridded Climate Database, and spatial data from government bodies, to assess relationships between pied crow population and range changes, land use, infrastructure, urbanisation and climate change.ResultsPied crow numbers have increased significantly in the past three decades, but rate of increase varied geographically, with crows declining in the northeast and increasing in the south-west of South Africa. Pied crow population changes were strongly correlated with climate change. Crows have benefited most from climate warming in the shrubland biomes of south-western South Africa. Pied crows are tree nesters, and within these shrublands, there is a strong positive relationship between the rate of population increase and the density of powerline infrastructure, which may facilitate pied crows’ increase by providing nesting sites.Main conclusionsPied crow numbers have increased in response to climate warming, with their spread facilitated by electrical infrastructure in south-western South Africa, providing a clear example of compound influence of multiple global change drivers promoting a significant change in species range and reporting rate. Pied crows are generalist predators and there is popular concern about their ecological impact in areas where increases have occurred. We highlight the importance of understanding the ecosystem-level implications of increased numbers of pied crows in South Africa's shrubland biomes.

One of my friends, Jamie Samson, has just had a paper published and it's pretty cool. He work on Cape ground squirrels, an animal that sends most of its day just calmly searching for food around their large burrows and then occasionally go crazy and have fights that could be scenes from the Matrix. These guys stash food away to save it for later in a behaviour known as caching. What Jamie found was that they pay attention to who is looking when they do it, to avoid being seen. This makes sense, as they can avoid their caches being stolen, but Jamie also found that the dominance rank impacted caching behaviour. Dominant individuals were less concerned with being observed than subordinates. It's cool work that builds on other investigations of caching species like scrub jays.

Samson & Manser (2015) Caching in the presence of competitors: Are Cape ground squirrels (Xerus inauris) sensitive to audience attentiveness? Animal Cognition When social animals cache food close to their burrow, the potential for an audience member to observe the event is significantly increased. As a consequence, in order to reduce theft it may be advantageous for animals to be sensitive to certain audience cues, such as whether they are attentive or not to the cache event. In this study, observations were made on three groups of Cape ground squirrels (Xerus inauris) in their natural habitat when they cached provisioned food items. When individuals cached within 10 m of conspecifics, we recorded the attentiveness (i.e. whether any audience members were orientated towards the cacher, had direct line of site and were not engaged in other activities) and identity of audience members. Overall, there was a preference to cache when audience members were inattentive rather than attentive. Additionally, we found rank effects related to cache avoidance whereby high-ranked individuals showed less avoidance to cache when audience members were attentive compared to medium- and low-ranked individuals. We suggest this audience sensitivity may have evolved in response to the difference in competitive ability amongst the ranks in how successful individuals are at winning foraging competitions. This study demonstrates that Cape ground squirrels have the ability to not only monitor the presence or absence of conspecifics but also discriminate individuals on the basis of their attentive state.LINK

A new paper from Dave Humphries on the pied babblers, looking at sexual displays from subordinates.Humphries et al (2015) Calling Where It Counts: Subordinate Pied Babblers Target the Audience of Their Vocal Advertisements. PLoS One, DOI: 10.1371/journal.pone.0130795Abstract:For territorial group-living species, opportunities to reproduce on the natal territory can be limited by a number of factors including the availability of resources within a territory, access to unrelated individuals, and monopolies on reproduction by dominant group members. Individuals looking to reproduce are therefore faced with the options of either waiting for a breeding opportunity to arise in the natal territory, or searching for reproductive opportunities in non-natal groups. In the cooperatively breeding Southern pied babbler, Turdoides bicolor, most individuals who achieve reproductive success do so through taking up dominant breeding positions within non-natal groups. For subordinate pied babblers therefore, searching for breeding opportunities in non-natal groups is of primary importance as this represents the major route to reproductive success. However, prospecting (where individuals leave the group to search for reproductive opportunities within other groups) is costly and individuals rapidly lose weight when not part of a group. Here we demonstrate that subordinate pied babblers adopt an alternative strategy for mate attraction by vocal advertisement from within their natal territories. We show that subordinates focus their calling efforts on the edges of their territory, and specifically near boundaries with neighbouring groups that have potential breeding partners (unrelated individuals of the opposite sex). In contrast to prospecting, calling individuals showed no body mass loss associated with this behaviour, suggesting that calling from within the group may provide a ‘cheap’ advertisement strategy. Additionally, we show that subordinates use information regarding the composition of neighbouring groups to target the greatest number of potential mating partners.LINK

One of my old colleagues, who's just finishing up his PhD has just had a paper published. James Westrip, supervised by Matt Bell, is working on interspecific communication through the pied babblers. Here's the abstract for the paper and a link to it:

Studying heterospecific communication provides an opportunity to examine the dynamics of cross-species social behaviour. It allows us to ask questions about the extent to which the transfer of information is adaptive or accidental and provides an empirically tractable context for manipulating relationships. To date, most studies of heterospecific communication have focussed on receivers. However, the selective pressures on signallers can be as important in determining the dynamics of interspecific communication. Here, we propose a simple framework for thinking about cross-species information transfer, which (i) considers whether information exchange is either accidental or adaptive and (ii) whether it is unidirectional or bidirectional. To clearly classify interactions, it is necessary to quantify all of the payoffs of interspecific communication to both signallers and receivers. This requires accurate characterisation of the currency influenced by cross-species communication (e.g. weight gain, foraging success, survival). However, quantifying the payoffs may be difficult, because each side may be benefiting via different currencies. To date, studies on heterospecific communication have focussed on only one dimension of a niche (usually antipredator or foraging signals). However, because niches are multidimensional, investigations should incorporate multiple aspects of a species’ niche, to get a better perspective on why we see certain patterns of information use between species.